Avian Introgression Patterns are Consistent With Haldane’s Rule

Abstract

According to Haldane’s Rule, the heterogametic sex will show the greatest fitness reduction in a hybrid cross. In birds, where sex is determined by a ZW-system, female hybrids are expected to experience lower fitness compared to male hybrids. This pattern has indeed been observed in several bird groups, but it is unknown whether the generality of Haldane’s Rule also extends to the molecular level. First, given the lower fitness of female hybrids, we can expect maternally inherited loci (i.e. mitochondrial and W-linked loci) to show lower introgression rates than biparentally inherited loci (i.e. autosomal loci) in females. Second, the faster evolution of Z-linked loci compared to autosomal loci and the hemizygosity of the Z-chromosome in females might speed up the accumulation of incompatible alleles on this sex chromosome, resulting in lower introgression rates for Z-linked loci than for autosomal loci. I tested these expectations by conducting a literature review which focused on studies that directly quantified introgression rates for autosomal, sex-linked and mitochondrial loci. Although most studies reported introgression rates in line with Haldane’s Rule, it remains important to validate these genetic patterns with estimates of hybrid fitness and supporting field observations to rule out alternative explanations. Genomic data provide exciting opportunities to obtain a more fine-grained picture of introgression rates across the genome, which can consequently be linked to ecological and behavioral observations, potentially leading to novel insights into the genetic mechanisms underpinning Haldane’s Rule.

Chromosome fissions and fusions act as barriers to gene flow betweenBrenthisfritillary butterflies

“…) then barrier loci, both recessive and dominant, may accumulate faster. Reduced gene flow on the Brenthis Z chromosome mirrors findings in other butterfly systems (Xiong et al 2022;Rosser et al 2022), as well as in birds (Irwin 2018;Ottenburghs 2022), suggesting that Z chromosomes often accumulate reproductive isolation at a faster rate than autosomes. Given that there are likely many barriers to gene flow between B. daphne and B. ino, especially on the Z, it may be inaccurate to describe the history of these species as 'chromosomal speciation'.…”

“…2022; Rosser et al . 2022), as well as in birds (Irwin 2018; Ottenburghs 2022), suggesting that Z chromosomes often accumulate reproductive isolation at a faster rate than autosomes. Given that there are likely many barriers to gene flow between B. daphne and B. ino , especially on the Z, it may be inaccurate to describe the history of these species as ‘chromosomal speciation’.…”

Hybridization in birds-of-paradise: Widespread ancestral gene flow despite strong sexual selection in a lek-mating system

“…The four bipartitions at the base of the core bird-of-paradise radiation (excluding Parotia ) have the lowest wCF and sCF scores across the phylogeny ( Figure S7 B); they coincide with strong incongruence between Z/A topologies and the frequency of competing topologies remains relatively stable along the 10 macrochromosomes. Variation in the tempo and mode of differentiation between Z/A is common in birds 42 and both the “fast-Z” and “large-Z” effect are often invoked as possible explanations. However, elevated differentiation on the Z chromosome is not necessarily driven by “adaptation” or “reproductive isolation,” and can also be the outcome of accelerated drift due to low Ne.…”

Mottled ducks, feral mallards, and their hybrids in Florida

“…According to Haldane's rule, hybrid female birds are expected to have less fitness than hybrid males. A meta‐analysis of 30 studies testing Haldane's rule in avian species revealed that 90% adhered to the rule (Ottenburghs 2022). When studying captive waterfowl, Kirby et al (2004) observed that most (65–66%) of the F 1 hybrid offspring of American black ducks and mallards were male.…”